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Erschienen in: Clinical Neuroradiology 3/2017

25.04.2016 | Original Article

The Hijdra scale has significant prognostic value for the functional outcome of Fisher grade 3 patients with subarachnoid hemorrhage

verfasst von: Julia S. Bretz, Falk Von Dincklage, MD, Johannes Woitzik, MD, Maren K. L. Winkler, MD, Sebastian Major, MD, Jens P. Dreier, MD Phd, Georg Bohner, MD, Michael Scheel, MD

Erschienen in: Clinical Neuroradiology | Ausgabe 3/2017

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Abstract

Purpose

Despite its high prevalence among patients with aneurysmal subarachnoid hemorrhage (aSAH) and high risk of delayed cerebral ischemia (DCI), the Fisher grade 3 category remains a poorly studied subgroup. The aim of this cohort study has been to investigate the prognostic value of the Hijdra sum scoring system for the functional outcome in patients with Fisher grade 3 aSAH, in order to improve the risk stratification within this Fisher category.

Methods

Initial CT scans of 72 prospectively enrolled patients with Fisher grade 3 aSAH were analyzed, and cisternal, ventricular, and total amount of blood were graded according to the Hijdra scale. Additionally, space-occupying subarachnoid blood clots were assessed. Outcome was evaluated after 6 months.

Results

Within the subgroup of Fisher grade 3, aSAH patients with an unfavorable outcome showed a significantly larger cisternal Hijdra sum score (HSS: 21.1 ± 5.2) than patients with a favorable outcome (HSS: 17.6 ± 5.9; p = 0.009). However, both the amount of ventricular blood (p = 0.165) and space-occupying blood clots (p = 0.206) appeared to have no prognostic relevance. After adjusting for the patient’s age, gender, tobacco use, clinical status at admission, and presence of intracerebral hemorrhage, the cisternal and total HSS remained the only independent parameters included in multivariate logistic regression models to predict functional outcome (p < 0.01).

Conclusion

The cisternal Hijdra score is fairly easy to perform and the present study indicates that it has an additional predictive value for the functional outcome within the Fisher 3 category. We suggest that the Hijdra scale is a practically useful prognostic instrument for the risk evaluation after aSAH and should be applied more often in the clinical setting.
Literatur
1.
Zurück zum Zitat Kramer AH, Hehir M, Nathan B, Gress D, Dumont AS, Kassell NF, Bleck TP. A comparison of 3 radiographic scales for the prediction of delayed ischemia and prognosis following subarachnoid hemorrhage. J Neurosurg. 2008;109:199–207.CrossRefPubMed Kramer AH, Hehir M, Nathan B, Gress D, Dumont AS, Kassell NF, Bleck TP. A comparison of 3 radiographic scales for the prediction of delayed ischemia and prognosis following subarachnoid hemorrhage. J Neurosurg. 2008;109:199–207.CrossRefPubMed
2.
Zurück zum Zitat Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.CrossRefPubMed Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.CrossRefPubMed
3.
Zurück zum Zitat van Norden AGW, van Dijk GW, van Huizen MD, Algra A, Rinkel GJE. Interobserver agreement and predictive value for outcome of two rating scales for the amount of extravasated blood after aneurysmal subarachnoid haemorrhage. J Neurol. 2006;253:1217–20.CrossRefPubMed van Norden AGW, van Dijk GW, van Huizen MD, Algra A, Rinkel GJE. Interobserver agreement and predictive value for outcome of two rating scales for the amount of extravasated blood after aneurysmal subarachnoid haemorrhage. J Neurol. 2006;253:1217–20.CrossRefPubMed
4.
Zurück zum Zitat Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J. Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke. 1990;21:1156–61.CrossRefPubMed Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J. Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke. 1990;21:1156–61.CrossRefPubMed
5.
Zurück zum Zitat Jiménez-Roldán L, Alén JF, Gómez PA, Lobato RD, Ramos A, Munarriz PM, Lagares A. Volumetric analysis of subarachnoid hemorrhage: assessment of the reliability of two computerized methods and their comparison with other radiographic scales. J Neurosurg. 2013;118:84–93.CrossRefPubMed Jiménez-Roldán L, Alén JF, Gómez PA, Lobato RD, Ramos A, Munarriz PM, Lagares A. Volumetric analysis of subarachnoid hemorrhage: assessment of the reliability of two computerized methods and their comparison with other radiographic scales. J Neurosurg. 2013;118:84–93.CrossRefPubMed
6.
Zurück zum Zitat Dupont SA, Wijdicks EFM, Manno EM, Lanzino G, Rabinstein AA. Prediction of angiographic vasospasm after aneurysmal subarachnoid hemorrhage: value of the Hijdra sum scoring system. Neurocrit Care. 2009;11:172–6.CrossRefPubMed Dupont SA, Wijdicks EFM, Manno EM, Lanzino G, Rabinstein AA. Prediction of angiographic vasospasm after aneurysmal subarachnoid hemorrhage: value of the Hijdra sum scoring system. Neurocrit Care. 2009;11:172–6.CrossRefPubMed
7.
Zurück zum Zitat Friedman JA, Goerss SJ, Meyer FB, Piepgras DG, Pichelmann MA, McIver JI, Toussaint LG, McClelland RL, Nichols DA, Atkinson JLD, Wijdicks EFM. Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: a novel approach to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg. 2002;97:401–7.CrossRefPubMed Friedman JA, Goerss SJ, Meyer FB, Piepgras DG, Pichelmann MA, McIver JI, Toussaint LG, McClelland RL, Nichols DA, Atkinson JLD, Wijdicks EFM. Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: a novel approach to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg. 2002;97:401–7.CrossRefPubMed
8.
Zurück zum Zitat Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, Crevel H. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke. 1988;19:1250–6.CrossRefPubMed Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, Crevel H. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke. 1988;19:1250–6.CrossRefPubMed
9.
Zurück zum Zitat Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES Jr., MacDonald RL, Mayer SA. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery. 2006;59:21–7.CrossRefPubMed Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES Jr., MacDonald RL, Mayer SA. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery. 2006;59:21–7.CrossRefPubMed
10.
Zurück zum Zitat Wilson DA, Nakaji P, Abla AA, Uschold TD, Fusco DJ, Oppenlander ME, Albuquerque FC, McDougall CG, Zabramski JM, Spetzler RF. A simple and quantitative method to predict symptomatic vasospasm after subarachnoid hemorrhage based on computed tomography: beyond the Fisher scale. Neurosurgery. 2012;71:869–75.CrossRefPubMed Wilson DA, Nakaji P, Abla AA, Uschold TD, Fusco DJ, Oppenlander ME, Albuquerque FC, McDougall CG, Zabramski JM, Spetzler RF. A simple and quantitative method to predict symptomatic vasospasm after subarachnoid hemorrhage based on computed tomography: beyond the Fisher scale. Neurosurgery. 2012;71:869–75.CrossRefPubMed
11.
Zurück zum Zitat Rosen DS, Amidei C, Tolentino J, Reilly C, Macdonald RL. Subarachnoid clot volume correlates with age, neurological grade, and blood pressure. Neurosurgery. 2007;60:259–267.CrossRefPubMed Rosen DS, Amidei C, Tolentino J, Reilly C, Macdonald RL. Subarachnoid clot volume correlates with age, neurological grade, and blood pressure. Neurosurgery. 2007;60:259–267.CrossRefPubMed
12.
Zurück zum Zitat Rosen DS, Macdonald RL, Huo D, Goldenberg FD, Novakovic RL, Frank JI, Rosengart AJ. Intraventricular hemorrhage from ruptured aneurysm: clinical characteristics, complications, and outcomes in a large, prospective, multicenter study population. J Neurosurg. 2007;107:261–5.CrossRefPubMed Rosen DS, Macdonald RL, Huo D, Goldenberg FD, Novakovic RL, Frank JI, Rosengart AJ. Intraventricular hemorrhage from ruptured aneurysm: clinical characteristics, complications, and outcomes in a large, prospective, multicenter study population. J Neurosurg. 2007;107:261–5.CrossRefPubMed
13.
Zurück zum Zitat Ko SB, Choi HA, Carpenter AM, Helbok R, Schmidt JM, Badjatia N, Claassen J, Connolly ES, Mayer SA, Lee K. Quantitative analysis of hemorrhage volume for predicting delayed cerebral Ischemia after Subarachnoid hemorrhage. Stroke. 2011;42:669–74.CrossRefPubMed Ko SB, Choi HA, Carpenter AM, Helbok R, Schmidt JM, Badjatia N, Claassen J, Connolly ES, Mayer SA, Lee K. Quantitative analysis of hemorrhage volume for predicting delayed cerebral Ischemia after Subarachnoid hemorrhage. Stroke. 2011;42:669–74.CrossRefPubMed
14.
Zurück zum Zitat Gurusinghe NT, Richardson AE. The value of computerized tomography in aneurysmal subarachnoid hemorrhage. J Neurosurg. 1984;60:763–70.CrossRefPubMed Gurusinghe NT, Richardson AE. The value of computerized tomography in aneurysmal subarachnoid hemorrhage. J Neurosurg. 1984;60:763–70.CrossRefPubMed
15.
Zurück zum Zitat De Rooij NK, Greving JP, Rinkel GJE, Frijns CJM. Early prediction of delayed cerebral ischemia after subarachnoid hemorrhage: development and validation of a practical risk chart. Stroke. 2013;44:1288–94.CrossRefPubMed De Rooij NK, Greving JP, Rinkel GJE, Frijns CJM. Early prediction of delayed cerebral ischemia after subarachnoid hemorrhage: development and validation of a practical risk chart. Stroke. 2013;44:1288–94.CrossRefPubMed
17.
Zurück zum Zitat Nieuwkamp DJ, Setz LE, Algra A, Linn FHH, de Rooij NK, Rinkel GJE. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8:635–42.CrossRefPubMed Nieuwkamp DJ, Setz LE, Algra A, Linn FHH, de Rooij NK, Rinkel GJE. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8:635–42.CrossRefPubMed
18.
Zurück zum Zitat Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.CrossRefPubMed Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.CrossRefPubMed
19.
Zurück zum Zitat Smith ML, Abrahams JM, Chandela S, Smith MJ, Hurst RW, Le Roux PD. Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited. Surg Neurol. 2005;63:229–234.CrossRefPubMed Smith ML, Abrahams JM, Chandela S, Smith MJ, Hurst RW, Le Roux PD. Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited. Surg Neurol. 2005;63:229–234.CrossRefPubMed
20.
Zurück zum Zitat Drenckhahn C, Brabetz C, Major S, Wiesenthal D, Woitzik J, Dreier JP, COSBID Study Group. Criteria for the diagnosis of noninfectious and infectious complications after aneurysmal subarachnoid hemorrhage in DISCHARGE-1. Acta Neurochir Suppl. 2013;115:153–9.PubMed Drenckhahn C, Brabetz C, Major S, Wiesenthal D, Woitzik J, Dreier JP, COSBID Study Group. Criteria for the diagnosis of noninfectious and infectious complications after aneurysmal subarachnoid hemorrhage in DISCHARGE-1. Acta Neurochir Suppl. 2013;115:153–9.PubMed
21.
Zurück zum Zitat van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7.CrossRefPubMed van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7.CrossRefPubMed
22.
Zurück zum Zitat Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.CrossRefPubMed Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.CrossRefPubMed
23.
Zurück zum Zitat Woertgen C, Ullrich OW, Rothoerl RD, Brawanski A. Comparison of the Claassen and Fisher CT classification scale to predict ischemia after aneurysmatic SAH? Zentralbl Neurochir. 2003;64:104–8.CrossRefPubMed Woertgen C, Ullrich OW, Rothoerl RD, Brawanski A. Comparison of the Claassen and Fisher CT classification scale to predict ischemia after aneurysmatic SAH? Zentralbl Neurochir. 2003;64:104–8.CrossRefPubMed
24.
Zurück zum Zitat Mayfrank L, Hütter BO, Kohorst Y, Kreitschmann-Andermahr I, Rohde V, Thron A, Gilsbach JM. Influence of intraventricular hemorrhage on outcome after rupture of intracranial aneurysm. Neurosurg Rev. 2001;24:185–91.CrossRefPubMed Mayfrank L, Hütter BO, Kohorst Y, Kreitschmann-Andermahr I, Rohde V, Thron A, Gilsbach JM. Influence of intraventricular hemorrhage on outcome after rupture of intracranial aneurysm. Neurosurg Rev. 2001;24:185–91.CrossRefPubMed
25.
Zurück zum Zitat Brouwers PJ, Dippel DW, Vermeulen M, Lindsay KW, Hasan D, van Gijn J. Amount of blood on computed tomography as an independent predictor after aneurysm rupture. Stroke. 1993;24:809–14.CrossRefPubMed Brouwers PJ, Dippel DW, Vermeulen M, Lindsay KW, Hasan D, van Gijn J. Amount of blood on computed tomography as an independent predictor after aneurysm rupture. Stroke. 1993;24:809–14.CrossRefPubMed
26.
Zurück zum Zitat Czorlich P, Ricklefs F, Reitz M, Vettorazzi E, Abboud T, Regelsberger J, Westphal M, Schmidt NO. Impact of intraventricular hemorrhage measured by Graeb and LeRoux score on case fatality risk and chronic hydrocephalus in aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2015;157:409–15.CrossRef Czorlich P, Ricklefs F, Reitz M, Vettorazzi E, Abboud T, Regelsberger J, Westphal M, Schmidt NO. Impact of intraventricular hemorrhage measured by Graeb and LeRoux score on case fatality risk and chronic hydrocephalus in aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2015;157:409–15.CrossRef
27.
Zurück zum Zitat Kramer AH, Mikolaenko I, Deis N, Dumont AS, Kassell N, Bleck TP, Nathan BA. Intraventricular hemorrhage volume predicts poor outcomes but not delayed ischemic neurological deficits among patients with ruptured cerebral aneurysms. Neurosurgery. 2010;67:1044–53.CrossRefPubMed Kramer AH, Mikolaenko I, Deis N, Dumont AS, Kassell N, Bleck TP, Nathan BA. Intraventricular hemorrhage volume predicts poor outcomes but not delayed ischemic neurological deficits among patients with ruptured cerebral aneurysms. Neurosurgery. 2010;67:1044–53.CrossRefPubMed
28.
Zurück zum Zitat Roos YB, Hasan D, Vermeulen M. Outcome in patients with large intraventricular haemorrhages: a volumetric study. J Neurol Neurosurg Psychiatr. 1995;58:622–4.CrossRefPubMedPubMedCentral Roos YB, Hasan D, Vermeulen M. Outcome in patients with large intraventricular haemorrhages: a volumetric study. J Neurol Neurosurg Psychiatr. 1995;58:622–4.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Niikawa S, Kitajima H, Ohe N, Miwa Y, Ohkuma A. Significance of acute cerebral swelling in patients with sylvian hematoma due to ruptured middle cerebral artery aneurysm, and its management. Neurol Med Chir Tokyo. 1998;38:844–50.CrossRefPubMed Niikawa S, Kitajima H, Ohe N, Miwa Y, Ohkuma A. Significance of acute cerebral swelling in patients with sylvian hematoma due to ruptured middle cerebral artery aneurysm, and its management. Neurol Med Chir Tokyo. 1998;38:844–50.CrossRefPubMed
30.
Zurück zum Zitat Güresir E, Beck J, Vatter H, Setzer M, Gerlach R, Seifert V, Raabe A. Subarachnoid hemorrhage and intracerebral hematoma: incidence, prognostic factors, and outcome. Neurosurgery. 2008;63:1088–94.CrossRefPubMed Güresir E, Beck J, Vatter H, Setzer M, Gerlach R, Seifert V, Raabe A. Subarachnoid hemorrhage and intracerebral hematoma: incidence, prognostic factors, and outcome. Neurosurgery. 2008;63:1088–94.CrossRefPubMed
31.
Zurück zum Zitat Hauerberg J, Eskesen V, Rosenørn J. The prognostic significance of intracerebral haematoma as shown on CT scanning after aneurysmal subarachnoid haemorrhage. Br J Neurosurg. 1994;8:333–9.CrossRefPubMed Hauerberg J, Eskesen V, Rosenørn J. The prognostic significance of intracerebral haematoma as shown on CT scanning after aneurysmal subarachnoid haemorrhage. Br J Neurosurg. 1994;8:333–9.CrossRefPubMed
32.
Zurück zum Zitat Bruder M, Schuss P, Berkefeld J, Wagner M, Vatter H, Seifert V, Güresir E. Subarachnoid hemorrhage and intracerebral hematoma caused by aneurysms of the anterior circulation: influence of hematoma localization on outcome. Neurosurg Rev. 2014;37:653–9.CrossRefPubMed Bruder M, Schuss P, Berkefeld J, Wagner M, Vatter H, Seifert V, Güresir E. Subarachnoid hemorrhage and intracerebral hematoma caused by aneurysms of the anterior circulation: influence of hematoma localization on outcome. Neurosurg Rev. 2014;37:653–9.CrossRefPubMed
33.
Zurück zum Zitat Haug T, Sorteberg A, Sorteberg W, Lindegaard K‑F, Lundar T, Finset A. Cognitive outcome after aneurysmal subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological, and management parameters. Neurosurgery. 2007;60:649–56, discussion 656–7.CrossRefPubMed Haug T, Sorteberg A, Sorteberg W, Lindegaard K‑F, Lundar T, Finset A. Cognitive outcome after aneurysmal subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological, and management parameters. Neurosurgery. 2007;60:649–56, discussion 656–7.CrossRefPubMed
34.
Zurück zum Zitat Greebe P, Rinkel GJE, Hop JW, Visser-Meily JMA, Algra A. Functional outcome and quality of life 5 and 12.5 years after aneurysmal subarachnoid haemorrhage. J Neurol. 2010;257:2059–64.CrossRefPubMedPubMedCentral Greebe P, Rinkel GJE, Hop JW, Visser-Meily JMA, Algra A. Functional outcome and quality of life 5 and 12.5 years after aneurysmal subarachnoid haemorrhage. J Neurol. 2010;257:2059–64.CrossRefPubMedPubMedCentral
Metadaten
Titel
The Hijdra scale has significant prognostic value for the functional outcome of Fisher grade 3 patients with subarachnoid hemorrhage
verfasst von
Julia S. Bretz
Falk Von Dincklage, MD
Johannes Woitzik, MD
Maren K. L. Winkler, MD
Sebastian Major, MD
Jens P. Dreier, MD Phd
Georg Bohner, MD
Michael Scheel, MD
Publikationsdatum
25.04.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Neuroradiology / Ausgabe 3/2017
Print ISSN: 1869-1439
Elektronische ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-016-0509-0

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